Bottom Line:
Our results suggest that the identified proteins and biomimetic polypeptides influence nucleation in vitro.Even though the in vivo role cannot be directly determined from our experiments, we can rationalize the following design principles: proteins, larger complexes, or membrane components that promote nucleation in vivo are likely to expose positively charged residues to a negatively charged crystal surface.In turn, components with acidic (negatively charged) functionality are nucleation inhibitors, which stabilize an amorphous structure through the coordination of iron.

ABSTRACTBiological materials typically display complex morphologies and hierarchical architectures, properties that are hardly matched by synthetic materials. Understanding the biological control of mineral properties will enable the development of new synthetic approaches toward biomimetic functional materials. Here, we combine biocombinatorial approaches with a proteome homology search and in vitro mineralization assays to assess the role of biological determinants in biomimetic magnetite mineralization. Our results suggest that the identified proteins and biomimetic polypeptides influence nucleation in vitro. Even though the in vivo role cannot be directly determined from our experiments, we can rationalize the following design principles: proteins, larger complexes, or membrane components that promote nucleation in vivo are likely to expose positively charged residues to a negatively charged crystal surface. In turn, components with acidic (negatively charged) functionality are nucleation inhibitors, which stabilize an amorphous structure through the coordination of iron.

fig3: Particlesize distribution of magnetite particles formed in thepresence of polyR.

Mentions:
polyR serves as a proxy for apotential polycationic biomolecular structure as inferred from theearlier literature reports by Barbas et al. and Brown et al.27,28 Coprecipitation of ferrous and ferric iron (at Fe3+/Fe2+ = 2/1) under alkaline conditions at pH ≥9 yieldscrystalline magnetite with grain sizes dependent on the alkalinity.34,35 Under these conditions, polyR affects the size, morphology, andaggregation behavior of the formed magnetite nanoparticles: in itspresence, we obtained monodisperse, stable single-domain-sized nanoparticlesof 35 ± 5 nm (Figure 3) that assembleto chain structures in solution (up to several micrometers; Figures 2A and S4–S6 anda video). Despite their irregular morphology, particles are mostlysingle-crystalline (Figure 2C). The nucleationand colloidal stabilization effects of polyR, leading to particlechain formation in vitro, are similar to the colloidal stabilizationby magnetosome compartimentalization in the bacteria in vivo. Thiscompartimentalization is provided by a lipid membrane containing diversetransmembrane proteins of yet mostly unknown functions. Interestingly,the lipid composition of the magnetosomes is dominated by phosphatidylethanolamines.36 Such lipid layers therefore expose mainly positivelycharged amines toward the intracellular magnetite crystals in linewith our observation of a polyR-induced colloidal stabilization effect.

Bottom Line:
Our results suggest that the identified proteins and biomimetic polypeptides influence nucleation in vitro.Even though the in vivo role cannot be directly determined from our experiments, we can rationalize the following design principles: proteins, larger complexes, or membrane components that promote nucleation in vivo are likely to expose positively charged residues to a negatively charged crystal surface.In turn, components with acidic (negatively charged) functionality are nucleation inhibitors, which stabilize an amorphous structure through the coordination of iron.

ABSTRACTBiological materials typically display complex morphologies and hierarchical architectures, properties that are hardly matched by synthetic materials. Understanding the biological control of mineral properties will enable the development of new synthetic approaches toward biomimetic functional materials. Here, we combine biocombinatorial approaches with a proteome homology search and in vitro mineralization assays to assess the role of biological determinants in biomimetic magnetite mineralization. Our results suggest that the identified proteins and biomimetic polypeptides influence nucleation in vitro. Even though the in vivo role cannot be directly determined from our experiments, we can rationalize the following design principles: proteins, larger complexes, or membrane components that promote nucleation in vivo are likely to expose positively charged residues to a negatively charged crystal surface. In turn, components with acidic (negatively charged) functionality are nucleation inhibitors, which stabilize an amorphous structure through the coordination of iron.